Flexible growth and body mass predict physiological condition at fledging in the synchronously breeding European starling, Sturnus vulgaris

Abstract

Recent studies have reported beneficial carryover effects of juvenile development that predict interspecific survival differences at independence. Yet, traits relating to body size (i.e. morphological traits) have proven to be unreliable predictors of juvenile survival within species. Exploring individual variation of growth trajectories and how they covary with physiology could reveal species-specific developmental modes which have implications for our assessments of juvenile quality. Here, we investigated morphological development of European starlings ( Sturnus vulgaris ) approaching fledging in relation to three components of physiological condition at independence: aerobic capacity, energy state and oxidative status. We found evidence of flexible mass and wing growth which independently covaried with fledgling energy state and aerobic capacity, respectively. By comparison, tarsus and wing length at fledging were unrelated to any physiological trait, while mass was positively associated with principal component scores that comprised aerobic capacity and energy state. Thus, flexible growth trajectories were consistent with ‘developmental plasticity’: adaptive pre-fledging mass recession and compensatory wing growth, which seemingly came at a physiological cost, while fledgling body mass positively reflected overall physiological condition. This highlights how patterns of growth and absolute size may differently reflect fledgling physiology, potentially leading to variable relationships between morphological traits and juvenile fitness.

Decoupling of body size, physiological state and subsequent performance in a developmentally manipulated songbird

“…This suggests mass-independent, and potentially hardwired, development of some physiological traits in species with non-linear developmental profiles. Increased dROMs in the treatment group might suggest an oxidative cost for such hardwired developmental trajectories (Costantini, 2016;Metcalfe & Alonso-Alvarez, 2010), since previous work in European starlings showed no direct relationship between dROMs and mass recession (Allen et al, 2022). Indeed, our results here suggest that increased free radical production in WT nestlings was not a consequence of development in a reduced energy state, contrary to our prediction.…”

“…Previous work has shown strong correlations between changes in mass and plasma triglycerides, which would be consistent with fat catabolism as a mechanism for mass recession (Allen et al, 2022). Our results here suggest that changes in mass and plasma triglycerides are simply correlated and the metabolization of energy stores is not a mechanism for mass recession.…”

“…We predicted that both aerobic capacity and energy state would co‐vary with changes in mass, yet the lack of variation in plasma triglycerides between treatment groups was particularly surprising. Previous work has shown strong correlations between changes in mass and plasma triglycerides, which would be consistent with fat catabolism as a mechanism for mass recession (Allen et al., 2022). Our results here suggest that changes in mass and plasma triglycerides are simply correlated and the metabolization of energy stores is not a mechanism for mass recession.…”

“…We assayed blood samples for five physiological traits, representing three metrics of physiological state: aerobic capacity (haematocrit and haemoglobin), energy state (plasma triglycerides), and oxidative status (dROMs and OXY). Standard assay methods were used to analyse blood samples (see Allen et al., 2022); we used a single pooled plasma sample to calculate intra‐ and inter‐assay coefficients of variation (CV). This pool was run on an initial quality control plate with 10 replicates (intra‐assay CV: haemoglobin = 0.9%; plasma triglycerides = 2.67%; OXY = 9.92%; dROMs = 4.77%) and alongside each subsequent plate (inter‐assay CV: haemoglobin = 2.27%; plasma triglycerides = 8.61%; OXY = 4.07%; dROMs = 11.2%).…”

“…We then assumed a developmental coupling of morphological and physiological traits, such that we predicted reduced physiological state in WT nestlings as a consequence of their expected lower body mass. More specifically, we predicted that WT nestlings would fledge with: (i) reduced aerobic capacity (lower haematocrit and haemoglobin), as experimentally decreased body mass (and thus, lower energy state; see below) would be associated with reduced developmental rate of physiological traits (Allen et al., 2022; Cuervo et al., 2011), (ii) decreased energy state (plasma triglycerides) resulting from facultative metabolisation of fat reserves as a mechanism for mass recession (Allen et al., 2022; Martins, 1997; Ricklefs, 1968) and (iii) decreased oxidative status (increased dROMs, decreased OXY), as development during lower energy states (i.e. poor developmental conditions) would increase the production of free radicals (e.g.…”